Urban Ecosyst (2006) 9: 351–359
DOI 10.1007/s11252-006-0005-4
Preliminary observations on habitat, support use and diet
in two non-native primates in an urban Atlantic forest
fragment: The capuchin monkey (Cebus sp.)
and the common marmoset (Callithrix jacchus)
in the Tijuca forest, Rio de Janeiro
André A. Cunha & Marcus V. Vieira & Carlos E. V. Grelle
Published online: 18 October 2006
# Springer Science + Business Media, LLC 2006
Abstract Space is an important dimension of the ecological niche. Differentiation in the
use of vertical strata of the forest is related to species body size, and explains in part species
coexistence at a local scale. Large neotropical primates dwell in the canopy, moving
quadrupedally on large branches, whereas smaller species leap between narrow branches in
the understory. We tested this general pattern by observing focal individuals of the capuchin
monkey (Cebus sp.) and the common marmoset (Callithrix jacchus), both non-native
species, living in a forest fragment within the Rio de Janeiro city. Results were in
accordance with the pattern for neotropical primates. Vertical use of the forest seems to be
related with ecological interactions, especially for C. jacchus restricted to the lower strata
due to aerial predation. Preliminary observations on diet corroborate the omnivory of Cebus
and the gum feeding characteristic of C. jacchus. For Cebus sp. the exotic jack-fruit
(Artocarpus heterophyllus) was the most important food item. Predation of both primates
on vertebrates, especially by C. jacchus on passerines, could cause an uncommon impact on
prey populations. In spite of anthropogenic impact, these non-native primates maintain the
general pattern of habitat, support use and diet of the same or similar species in native
neotropical communities.
Keywords Exotic species . Ecological niche . Vertical stratification . Locomotion . Diet .
Anti-predation behaviour . Atlantic forest . Neotropical primates . Mammals
Introduction
Space use is an important factor to understand species distribution and coexistence, which
can be perceived at different scales. For primates, for example, at a continental scale the
geographic range is an important factor in understanding species distribution (Rylands et al.,
A. A. Cunha (*) : M. V. Vieira : C. E. V. Grelle
Laboratório de Vertebrados, Programa de Pós-Graduação em Ecologia,
Departamento de Ecologia, Universidade Federal do Rio de Janeiro, Ilha do Fundão,
CCS, sala A2-084, CP 68020,
Rio de Janeiro, RJ. Brazil CEP 21941-590
e-mail: cunha.andre@gmail.com
352
Urban Ecosyst (2006) 9: 351–359
1996; Peres, 1997; Peres and Janson, 1999). Habitat association explains species occurrences and sympatries at a regional scale, (Rylands, 1987; Peres and Janson, 1999), and
vertical stratification in the forest allows the comprehension of coexistences and syntopies
at a local scale (Fleagle et al., 1981; Terborgh, 1983; Peres, 1993). These factors together
allow a detailed map of species distribution. In fact, space use was recognized as a fundamental dimension of the ecological niche (MacArthur, 1958; Connell, 1961; Schoener,
1974, 1983; Cunha and Vieira, 2004a). Differentiation in space use is a key factor in community structure, especially in three dimensional or complex environments (August, 1983;
Grelle, 2003) such as tropical forests.
Neotropical primates vary in habitat use, body size, vertical stratification and diet, and
considering all genera there is an extensive overlap in these niche dimensions (Table 1).
However, focusing on spatial scales (continental, regional and local), it is possible to
recognize specific spatial niches. Comparing available information for primate communities
between the Amazon and the Atlantic forest, there is a more detailed differentiation in the
vertical space use in the Amazon where four vertical strata are present (Table 1). However,
Atlantic forest remains only in slope terrains, where only the canopy and the understory are
clearly distinguishable and vertical differentiation seems to be coarser.
Overall, there is a clear relationship between body size and the height of strata used by the
species, its locomotor mode, diet, and diameters of branches and trunks used. Large species
occupy the highest strata, while small primates live mostly in the understory, and medium
ones in all strata but mainly in the intermediate strata (Table 1). Quadrupedal and suspensory
locomotor mode are typical for large neotropical primates, whereas for small species leaps
are the main locomotor mode (Reed, 1999). Large species use large supports in the arboreal
strata, and smaller species move mainly on small diameter branches. In diet, body size is
negatively related with faunivory and positively associated with leaves and fruits consumed
(Reed, 1999).
The Tijuca forest of Rio de Janeiro, Brazil, is one of the largest urban forests of the
world, located inside the city. It represents a unique system to test the pervasiveness of this
pattern of stratification related to body size in primates. This forest has a long history of
disturbance. Before the 16th century the region harbored a dense indigenous population.
With European colonization the real history of deforestation began, initially with the
logging of Brazil wood (Caeesalpinia echinata) in the 16th and 17th centuries. After the
commercial extinction of this tree, in the 18th and 19th centuries, almost half of the forest
cover was replaced by coffee plantations (Dean, 1996). The rivers feeding the city of Rio de
Janeiro dried up in the middle of 19th and the Emperor Dom Pedro II, recognizing the link
between deforestation and maintenance of headwaters, ordered the reforestation of the
Tijuca massif. The forest was restored with exotic and native trees (CCN, 1966). In the first
decades of 20th century, exotic vertebrates, including primates, were accidentally
introduced by runaways from a handling center of the environmental policy agency and
by release of tamed animals. Nowadays, Tijuca forest is characterized by numerous species
of non-native plants and animals.
The original primate community predictably included the southern muriqui (Brachyteles
arachnoides), the howler monkey (Alouatta guariba), the black-horned capuchin (Cebus
nigritus), the buffy-tufted ear marmoset (C. jacchus), and in lower elevations the goldenlion tamarin (Leontopithecus rosalia). Nowadays, the exotic common marmoset (C.
jacchus), and the capuchin monkey (Cebus sp.) are the more abundant primate species. The
Urban Ecosyst (2006) 9: 351–359
353
Table 1 Niche dimensions of diurnal neotropical primate genera
Genus
Sizea
Dietb
Habitats (forests)c
Vertical stratad
Amazon
Ateles
Large
Frugivorous–
folivorous
Frugivorous–
folivorous
Folivorous–
frugivorous
Frugivorous–
granivorous
Frugivorous–
granivorous
Frugivorous–
onivorous
Frugivorous–
granivorous
Frugivorous–
onivorous
Frugivorous–
onivorous
Insetivorous–
onivorous
Insetivorous–
onivorous
Insetivorous–
onivorous
Insetivorous–
onivorous
Terra firme
Low canopy, upper canopy,
emergents
Low canopy, upper canopy
Lagothrix
Large
Alouatta
Large
Cacajao
Medium
Pithecia
Medium
Cebus
Medium
Chiropotes
Medium
Callicebus
Medium
Saimiri
Small
Callimico
Small
Saquinus
Small
Mico
Small
Cebuella
Small
Atlantic forest
Brachyteles
Large
Alouatta
Large
Cebus
Medium
Callicebus
Medium
Leontopithecus
Small
Callithrix
Small
Frugivorous–
folivorous
Folivorous–
frugivorous
Frugivorous–
onivorous
Frugivorous–
onivorous
Insetivorous–
onivorous
Gumivorous–
onivorous
Terra firme
Várzea, terra firme
Terra firme
Low canopy, upper canopy,
emergents
Low canopy, upper canopy,
emergents
Understory, low canopy,
upper canopy
Understory, low canopy,
upper canopy, emergents
Low canopy, upper canopy,
emergents
Understory, low canopy,
upper canopy, emergents
Understory, low canopy,
upper canopy
Understory, low canopy
Terra firme
Understory, low canopy
Terra firme
Understory, low canopy
Terra firme
Understory, low canopy
Montane, semi-decidous
Canopy
Montane, semi-decidous,
lowland, araucária
Montane, semi-decidous,
lowland, gallery
Montane, semi-decidous,
lowland, gallery
Semi-decidous, lowland
Canopy
Montane, semi-decidous,
lowland, gallery
Understory, canopy
Várzea
Terra firme
Terra firme, Várzea
Terra firme
Terra firme
Várzea
Understory, canopy
Understory, canopy
Understory, canopy
a
From Fonseca et al. (1996), classiffying as large (>4 kg); medium (1–4 kg); and small (<1 kg).
b
Adapted from Fonseca et al. (1996).
c
According with Rylands et al. (1996) for Atlantic forest; and Peres (1997), and Peres and Dolman (2000)
for the Amazon.
d
According with Rylands et al. (1996) for Atlantic forest; and synthesized from Rylands (1987); Mendes
Pontes (1997); Peres (1997), and Peres and Dolman (2000) for the Amazon.
354
Urban Ecosyst (2006) 9: 351–359
Amazonian squirrel monkey (Saimiri) and the black-tufted-ear marmoset (Callithrix
penicillata) from Central Brazil also were reported to occur in the Tijuca forest, but were
not seen in the study area (Cunha and Vieira, 2004b). The capuchin individuals of Tijuca
forest have external morphological features resembling C. nigritus, C. libidinosus, C.
robustus forming probably a hybrid species (Cebus sp.) (Silva Jr., personal communication). If the pattern of vertical stratification related to body size is maintained in such a
unique and recent forest, it must be indeed a strong pattern.
We test this pattern of vertical stratification related to body size in this human built
primate community of the Tijuca forest. Based on focal observation, we intend to describe:
(1) the use of vertical space, (2) the main locomotory mode, (3) the diameters of supports
used, and (4) the food items consumed by the capuchin monkey and the common marmoset
in the Tijuca forest. Following Fleagle et al. (1981), we hypothesize that the larger species
(Cebus sp.) moves predominantly in the canopy, walking in a quadrupedal fashion. The
smaller marmoset is supposed to be detected mainly in the understory moving mainly by
leaping. In addition we also expect a positive relation between body size and diameters of
supports used. For diet, despite the factor of being introduced species, we expect that these
monkeys eat the same items they eat in areas were they are native. Thus Cebus sp. would be
more frugivorous, based on Freese and Oppenheimer (1981), whereas in accordance with
Stevenson and Rylands (1988) and Rylands and de Faria (1993), C. jacchus will be characterized as a typical gum-eating primate.
Material and methods
Study area
The Tijuca forest is a 9.340 ha forest fragment, where the 3.466 ha of the the Parque
Nacional da Tijuca is inserted. It is located inside the Rio de Janeiro city (22°55′–23°00′S e
43°11′–43°19′W), on the Tijuca massif, and represents an important area for tourism and
leisure for the city of Rio de Janeiro.
In spite of the history of coffee plantations until the 19th century, the general forest
structure and composition is of a typical secondary hill tropical rain forest, with palms,
ferns, epiphytes and lianas. Most frequent trees are Leguminosae, Sapotaceae, Bombacaceae, Euphorbiaceae, Meliaceae, Lauraceae, Lecythidaceae, Moraceae and Melastomataceae (CCN 1966). Canopy height varies from 10 to 20 m, with some emergent trees above
25 m, particulaly Cariniana estrellensis. At some sites there is a clear dominance in
biomass and structure of the exotic jackfruit (Artocarpus heterophyllus: Moraceae).
Field work was conducted from February to March and from July to August 2004 along
a 7.7 km paved road, ranging from 100 to 500 m above sea level, and beginning from the
edge to the interior of the forest fragment. The road was six meters wide with continuous
tree canopy above it. The transect was crossed eighteen times by bicycle with an average
speed of 3 km/h. Cunha (2005) estimated a population density of 100 to 177 Cebus sp. and
115 to 165 individuals/km2 C. jacchus in the Tijuca forest.
Data analysis
Visual census began between 06:00 h and 07:30 h and finished between 10:30 e 11:30 h a.m.
Encounters with groups lasted from 5 to 20 min. These primates are generally habituated to
Urban Ecosyst (2006) 9: 351–359
355
the presence of visitors, which frequently use the paved road to access other points of the
Tijuca forest. Besides, animals did not demonstrate any major behavioral change when
detected by the observer. In each encounter with a group the first adult observed was selected
as a focal individual (Altmann, 1974) and four variables (Table 2) were measured only once
in the following movement, avoiding problems of non-independent data. For diet
observation, only the first observation of the group was used, even if it was not from the
focal individual. The significance of differences in frequency of each category within each
variable were tested with chi-square one-tailed tests and Yates correction if necessary,
assuming as significant values of P < 0.05.
Results
Thirty six focal observations for Cebus sp. and 39 for C. jacchus were obtained. These
primates differed significantly in the use of the vertical space of the forest. Individuals of
Cebus sp. moved mostly in the canopy and less in the understory. Complementarily,
individuals of C. jacchus were frequently observed in the understory and seldom in the
canopy (Fig. 1a). Non-focal individuals were observed once on the ground for both species,
but were not considered for statistical analysis.
Locomotory modes were significantly diferent for Cebus sp. and C. jacchus (Fig. 1b).
Capuchins were quadrupedal, with few leaps observed for non-focal Cebus sp. and only by
young individuals crossing short distances (30–50 cm) between large supports (>20 cm).
Capuchin semi-prehensile tail was used in a few cases, once to help in the stabilization of
an individual trying to open a hard fruit, and also by young individuals playing. For the
common marmosets, leaping and quadrupedalism were the more frequent locomotory
modes. Considering focal individuals, only C. jacchus moved by leaps, reaching more than
two meters in some jumps.
Supports of all diameters were used by both primates. However, the frequency in each
diameter class differed significantly (Fig. 1c). The difference is related to body size. Cebus
sp. used large supports (>10 cm) in 70% of the observations. On the other hand, the smaller
C. jacchus used thinner branches (<10 cm) in 80% of the movements considered here.
Food items consumed also differed between these primates (Fig. 1d). Cebus sp. was
mainly frugivorous with around 60% of the observations made on fruits; invertebrates and
vertebrates were also consumed. Individuals of C. jacchus were mainly gum feeders,
secondarily searching for fruits and vertebrates. However, the most consumed fruit for both
species was the exotic jackfruit (A. heterophyllus) accounting for 65% of the fruits
consumed by C. jacchus and 80% for Cebus sp. In addition, these primates are potential
vertebrate predators (Fig. 1d), but consume or pursuit different items. The capuchin monkey
pursue Guianan squirrel (Sciurus aestuans) and ate chicken, whereas the common
Table 2 Variables measured in
the behavior observations of focal
individuals in the Tijuca forest,
Rio de Janeiro, RJ, Brazil
Variable
Categories
Vertical strata
Support diameter
(centimeters)
Locomotion mode
Food items
Ground, understory, canopy
0–5 cm, 5–10 cm, 10–30 cm, >30 cm
Quadrupedal, leap, climbing
Fruits, gum, invertebrates,
vertebrates
356
Urban Ecosyst (2006) 9: 351–359
a. Vertical Stratification
1
b. Locomotion Mode
1
Relative Frequency
Chi-s quare= 15.640 , P < 0.0001
0.8
0.8
0.6
0.6
0.4
0.4
0.2
0.2
0
Chi-s quare= 16.677 , P < 0.0002
0
Understory
Canopy
Quadrupedal
c. Support Diameter
Climbing
d. Food Itens
1
1
0.8
Leaping
Chi-s quare= 21.263 , P < 0.0001
0.8
0.6
0.6
0.4
0.4
0.2
0.2
Chi-s quare= 11.691 , P = 0.0085
0
0
0-5c m
5-10c m
10-30c m
>30c m
Fruits
Gum
Vert.
Invert.
Cebus sp.
Callithrix jacchus
Fig. 1 Relative frequencies of Cebus sp. and Callithrix jacchus using (a) the vertical strata (n = 34 and n =
37, respectively), (b) locomotory modes (n = 24 and n = 28, respectively), (c) support diameters (n = 24 and
n = 25, respectively), and (d) food items (n = 23 and n = 10, respectively) in the Tijuca Forest, Rio de
Janeiro, RJ, Brazil. One-tailed chi-square tests values were based on the comparison of absolute frequencies
marmoset pursue passerines in the understory (n = 2), such as the Myrmotherula
cyanocephala, and also in the canopy (n = 1), such as the Tangara sp. and other
Passeriformes.
Discussion
The capuchin monkey (Cebus sp.) and the common marmoset (C. jacchus) partition the
vertical space of Tijuca forest. In accordance with our hypothesis, these primates segregate
clearly in the use of vertical stratum, locomotion modes, diameters of supports used, and
also food items consumed. Common marmosets move by leaps in the understory on narrow
branches. On the other hand, the capuchin monkey dwells mostly in the canopy moving
quadrupedaly on large supports. Occasionally, both species climb down to the forest
ground. The vertical differentiation of sympatric primates in this study is in accordance with
the pattern observed for other neotropical primate communities (Fleagle and Mittermeier,
1980; Fleagle et al., 1981, Mittermeier and van Roosmalem, 1981; Charles-Dominique,
1983; Terborgh, 1983; Peres, 1993). In these studies larger species dwell in the canopy and
move quadrupedally, such as Cebus sp. in the Tijuca forest. On the other hand, smaller
species, such as C. jacchus in our study, move in the lower strata by leaps between the
supports discontinues of the understory of tropical forests (see Fleagle and Mittermeier,
1980 and Richards, 1998). Despite the history of intensive disturbance and potential
Urban Ecosyst (2006) 9: 351–359
357
differences in vegetation composition and structure, today the vegetation structure of the
Tijuca forest resembles other tropical forests, offering a similar arena for primates. As
expected, based on the literature, these primates use the vertical space of Tijuca forest
following the general pattern observed for neotropical primates (see Table 1).
Body sizes and the diameter of branches and trunks used were also related. Both species
move in all diameter supports. However, C. jacchus (weight ca.0,35 kg; Cunha,
unpublished data) used mainly narrow supports (<10 cm), and Cebus sp. (ca.3 kg,
Auricchio, 1995) used supports with more than 10 cm. A similar pattern was observed by
Fleagle et al. (1981) for sympatric Cebus apella and Saimiri sciureus in the Amazon, where
even in mixed troops these primates segregate clearly in the use of vertical space and
supports. Cunha and Vieira (2002) observed that larger Atlantic forest opossums used larger
supports more frequently than smaller species did. Thus, the positive relationship between
body size and diameter of supports used for arboreal species seems to be a general pattern,
at least for neotropical mammals.
Space use seems to be related to habitat structure and ecological interactions. The low
frequency of movements of Cebus sp. in the understory could be partially explained by
absence of continuous and larger supports, and also by preferential use of canopy, with
more abundant resources and supports (Richards, 1998).
Conversely, the high frequency of C. jacchus in the understory seems to be related to a
combination of an anti-aerial-predator behaviour, compressing this species to the lower
strata, and preference for smaller substrates. Hawks (Leucopternis lacernulata and
Rupornis magnirostris) were frequently observed in the study area, mostly at or near the
point of C. jacchus encounter (four out of five times). Aerial predation is an important
factor influencing marmoset’s movement behavior (Barrosa et al., 2004). Hawk calls induce
marmosets to adopt antipredator behaviors, such as freezing and searching for a safe
microhabitat (Searcy and Gaine, 2003). In the present study, two observations clearly
indicated the influence of raptors in the use of space by C. jacchus. The first was a group of
C. jacchus that promptly climbed down to hide under a dense understory foliage after a
white-necked-hawk (L. lacernulata) attack. The second observation was of two marmosets
hiding from a roadside hawk (R. magnirostris) perched in the understory. The two
marmosets were frozen behind the leaves of a shrub near the forest floor, one meter above
the ground and eight meters in front of the roadside hawk. Despite these observations, the
large percentage of time spent in the understory by marmosets also could be explained by
the preference for smaller supports, more abundant in this forest stratum. With no data on
support availability along the vertical space of the forest this issue will need a further study.
Overall, the association between understory use and leaping movements by small primates
described in other studies (Fleagle and Mittermeier, 1980; Fleagle et al., 1981; Rylands,
1987; Peres, 1993) was corroborated here.
Preliminary observations on diet also agree with previous studies. In this study Cebus sp.
were mainly frugivorous but also consumed animal items, corroborating the omnivore
characteristic of the genus. The diet of C. jacchus during the study period was mainly gum,
as expected for this species (Rylands et al., 1996; Rylands and de Faria, 1993). It also ate
fruits and animal items, specifically birds, but not insects as do other small neotropical
primates.
The consumption of passerines by the common marmoset would have an important
significance for the management of wildlife in this urban fragment. According to Stevenson
and Rylands (1988), marmosets rarely feed on birds and nestlings in its native habitats. But
in the Tijuca forest the consumption of birds by this exotic primate seems not to be so rare,
358
Urban Ecosyst (2006) 9: 351–359
as more than 20% of the prelimirary observations on foranging behaviour were bird
persecution, and actual adult bird consumption was also registered (J. Barroso, personal
communication). Capuchin monkeys could also be a threat to the vertebrate fauna of Tijuca
forest. Bird watchers attribute the apparent decline in the passerine abundance in the last
decades in the Rio de Janeiro Botanical Garden, contiguous to the study area, to primate
predation. Cunha (2005) suggests a possible overabundance of Cebus sp. and C. jacchus in
this fragment, which would increase the predation impact on the bird fauna.
Other evidence of the extreme adaptability of Cebus sp. was the consumption of a
chicken carcass on the forest ground. The consumption of small vertebrates is not frequent
for Cebus (Freese and Oppenheimer, 1981), but seems to be not as rare as for C. jacchus
(see Rose, 1997 and Resende et al., 2004). However carcass eating by Cebus spp. was not
in the literature. In addition, the high frequency of the exotic jackfruit (A. heterophyllus), in
Cebus sp. diet evidenciated the extreme adaptability of this genus.
Our preliminary observations on the diet of the capuchin monkey and common
marmoset in the Tijuca forest partially agrees with observations of Cebus and Callithrix in
other neotropical forests (Fleagle and Mittermeier, 1980; Rylands and de Faria, 1993), but
the intense faunivory of Callithrix pointed here was never reported. This unique aspect of
the diet could be related to the particular changes in composition and ecological interactions
compared to the past, original community, and to the high abundance of primate
populations in the Tijuca forest. These complex interactions between exotic and native
animal and plant species should be studied in detail and considered in any management
plan for this and other similar urban forest fragments.
In conclusion, the pattern of use of vertical space of the forest associated with body size
was corroborated in the modified neotropical Tijuca forest, indicating that this pattern must
be indeed general. Space use studies relating to species body sizes, support use, and
locomotion modes are fundamental to understand species interactions within a spatially
complex community. Trophic interaction studies between exotic and native species in the
human built Tijuca forest should be carried out to investigate the possible impact of these
primates on prey populations, especially on the bird fauna.
Aknowledgments We thanks Drs. Jean P. Boubli, Adriano G. Chiarello, Rui Cerqueira, Henrique Rajao and
anonymous reviewers for invaluable contributions on an earlier version of the manuscript. The Brazilian
Ministry of Education (CAPES) and Inter-American Bank of Development/Programa de Despoluição da
Baía de Guanabara/Fundação de Engenharia do Meio Ambiente/Instituto Terra de Preservação Ambiental
provided financial and logistical support.
References
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267
August PV (1983) Heterogeneity in structuring tropical mammal communities. Ecology 64:1495–1507
Auricchio P (1995) Primatas do Brasil. Terra Brasilis, São Paulo
Barrosa M, Alencar C, Tomaz C (2004) Differences in aerial and terrestrial visual scanning in captive black
tufted-ear marmoset (Callithrix penicillata) exposed to a novel environment. Folia Primatol 75:85–92
CCN (1966) Floresta da Tijuca. Rio de Janeiro, Centro de Conservação da Natureza
Charles-Dominique P (1983) Ecology and social adaptations in didelphid marsupials: comparison with
eutherians of similar ecology. Am Soc Mammal Spec Publ 7:395–422
Connell JH (1961) The influence of interspecific competition and other factors on the distribution of the
barnacle Chthamalus stellatus. Ecology 42:710–723
Cunha AA (2005) Estratificação vertical, abundância e tamanho populacional do macaco-prego (Cebus sp.)
e do mico-estrela (Callithrix jacchus) no Maciço da Tijuca, Rio de Janeiro, RJ, Brazil. MSc. thesis,
Universidade Federal do Rio de Janeiro, Rio de Janeiro
Urban Ecosyst (2006) 9: 351–359
359
Cunha AA, Vieira MV (2002) Support diameter, incline, and vertical movements of four didelphid
marsupials in the Atlantic forest of Brazil. J Zool 258:419–426
Cunha AA, Vieira MV (2004a) Two bodies cannot occupy the same place at the same time, or the
importance of space in the ecological niche. Bull Ecol Soc Am 85:25–26
Cunha AA, Vieira MV (2004b) Present and past primate community of the Tijuca forest, Rio de Janeiro,
Brazil. Neotrop Primates 12:153–154
Dean W (1996) A ferro e fogo: a história e a devastação da Mata Atlântica brasileira. São Paulo. Cia. das Letras
Fleagle JG, Mittermeier RA (1980) Locomotor behaviour, body size, and comparative ecology of seven
Surinam monkeys. Am J Phys Anthropol 52:301–314
Fleagle JG, Mittermeier RA, Skopec AL (1981) Different habitat use by Cebus apella and Saimiri sciureus
in central Surinam. Primates 22:361–367
Fonseca GAB, Herrmann G, Leite YLR, Mittermeier RA, Rylands AB, Patton J (1996) Lista Anotada
dos mamíferos do Brasil. Occ Pap Cons Biol 4:1–38
Freese CH, Oppenheimer JR (1981) The capuchin monkey, genus Cebus. In: Coimbra-Filho AF, Mittermeier
GC (eds) Ecology and behavior of neotropical primates. Academia Brasileira de Ciências, Rio de
Janeiro, pp 331–390
Grelle CE (2003) Forest structure and vertical stratification of small mammals in a secondary Atlantic forest,
southeastern, Brazil. Stud Neotrop Fauna Environ 38:81–85
MacArthur RH (1958) Population ecology of some warblers of northeastern coniferous forests. Ecology
39:599–619
Mendes Pontes AR (1997) Habitat partitioning among primates in Maracá Island, Roraima, Northen
Brazilian Amazonia. Int J Primatol 18:131–157
Mittermeier RA, van Roosmalem MGM (1981) Preliminary observation on habitat utilization and diet in
eight Surinam monkeys. Folia Primatol 36:1–39
Peres CA (1993) Structure and spatial organization of an Amazonia terra firme forest primate community.
J Trop Ecol 9:259–276
Peres CA (1997) Primate community structure at twenty western Amazonian flooded and unflooded forest.
J Trop Ecol 13:381–405
Peres CA, Dolman P (2000) Density compensation in neotropical primate communities: evidence from
56 hunted and non-hunted Amazonian forests of varying productivity. Oecologia 122:175–189
Peres CA, Janson CH (1999) Species coexistence, distribution and environmental determinants of neotropical primate richness: a community-level zoogeographic analysis. In: Fleagle JG, Janson C, Reed KE
(eds) Primate communities. Cambridge University Press, Cambridge, pp 55–74
Reed KE (1999) Population density of primates in communities: differences in community structure.
In: Fleagle JG, Janson C, Reed KE (eds) Primate communities. Cambridge University Press,
Cambridge, pp 116–140
Resende BD, Greco VLG, Ottoni EB, Izar P (2004) Some observations on the predation of small mammals
by the tufted capuchin (Cebus apella). Neotrop Primates 11:103–104
Richards PW (1998) The tropical rain forest: an ecological study. Cambridge University Press, Cambridge
Rose LM (1997) Vertebrate predation and food-sharing in Cebus and Pan. Int J Primat 18:727–765
Rylands AB (1987) Primate communities in Amazonian forests: their habitats and food resources.
Experientia 43:265–279
Rylands AB, de Faria DS (1993) Habitats, feeding ecology, and home range size in the genus Callithrix. In:
Rylands AB (ed) Marmosets and tamarins: systematics, behaviour, and ecology. Oxford Science
Publications, New York, pp 262–272
Rylands AB, Fonseca GAB, Leite YR, Mittermeier RA (1996) Primates of the Atlantic forest: origin,
distribution, endemism and communities. In: Norconk MA, Rosenberger AL, Garber PA (eds) Adaptive radiations of neotropical primates. Plenum, New York, pp 21–49
Schoener TW (1974) Resource partioning in ecological communities. Science 185:27–39
Schoener TW (1983) Field experiments on interspecific competition. Am Nat 122:240–285
Searcy YM, Gaine NG (2003) Hawk calls elicit alarm and defensive reactions in captive Geoffroy’s
marmosets (Callithrix geoffroyi). Folia Primatol 74:115–125
Stevenson MF, Rylands AB (1988) The marmosets, genus Callithrix. In: Mittermeier RA, Rylands AB,
Coimbra Filho AF, Fonseca GAB (eds) Ecology and behavior of neotropical primates, vol 2. World
Wildlife Fund, Washington, pp 131–222
Terborgh J (1983) Five new world primates: a study in comparative ecology. Princeton University Press,
New Jersey